Fluctuating asymmetry and exposure to pyrethroid insecticides in Triatoma infestans populations in northeastern Argentina

Exposure to sublethal doses of insecticide may affect biological traits in triatomines. We investigated the effects of toxicological phenotype (pyrethroid resistance status) and exposure to sublethal doses of deltamethrin on two traits of Triatoma infestans Klug (Heteroptera: Reduviidae) using a phenotypic plasticity experimental design. First-instar nymphs from 14 and 10 full-sib families from pyrethroid-susceptible and pyrethroid-resistant populations, respectively, were used. For the susceptible population, we treated first instars topically with acetone (control) or deltamethrin (treatment) once. For the resistant population, instars were treated once, twice and three times as first, third or fifth-instar nymphs, respectively. We measured cuticle thickness, wing size and wing shape of 484 emerging adults, and tested for treatment effects using mixed ANOVA and MANOVA models. Toxicological phenotype, exposure to deltamethrin and full-sib family exerted significant effects on cuticle thickness, wing size and wing shape. Adult triatomines previously treated with deltamethrin developed significantly thicker cuticles than control triatomines only in the resistant population and significantly bigger wings in both populations. Mean cuticle thickness and wing size increased with increasing exposures to deltamethrin. Exposure to sublethal doses of deltamethrin generated morphological modifications that may affect insect survival and flight dispersal, and hence may have evolutionary and epidemiological consequences.

Phenotypic plasticity, canalisation and developmental stability of Triatoma infestans wings: effects of a sublethal application of a pyrethroid insecticide

Abstract Background: Triatomine control campaigns have traditionally consisted of spraying the inside of houses with pyrethroid insecticides. However, exposure to sublethal insecticide doses after the initial application is a common occurrence and may have phenotypic consequences for survivors. Here, using Triatoma infestans (the main vector of Chagas disease in the Southern Cone of South America) as a model species, we quantifed the efects of exposure to a sublethal dose of pyrethroid insecticide on wing morphology. We tested if the treatment (i) induced a plastic efect (change in the character mean); (ii) altered environmental canalisation (higher individual variation within genotypes); (iii) altered genetic canalisation (higher variation among genotypes); and (iv) altered developmental stability (higher fuctuating asymmetry [FA]). Methods: Each of 25 full-sib families known to be susceptible to pyrethroid insecticides were split in two groups: one to be treated with a sublethal dose of deltamethrin (insecticide-treated group) and the other to be treated with pure acetone (control group). Wings of the emerging adults were used in a landmark-based geometric morphometry analysis to extract size and shape measurements. Average diferences among treatments were measured. Levels of variation among families, among individuals within families and among sides within individuals were computed and compared among treatments. Results: Wing size and shape were afected by a sublethal dose of deltamethrin. The treated insects had larger wings and a more variable wing size and shape than control insects. For both wing size and shape, genetic variation was higher in treated individuals. Individual variations and variations in FA were also greater in deltamethrin-treated insects than in control ones for all full-sib families; however, the patterns of shape variation associated with genetic variation, individual variation and FA were diferent. Conclusions: Insects exposed to a sublethal dose of deltamethrin presented larger, less symmetrical and less canalised wings. The insecticide treatment jointly impaired developmental stability and genetic and environmental canalisation. The divergent patterns of shape variation suggest that the related developmental bufering processes difered at least partially. The morphological modifcations induced by a single sublethal exposure to pyrethroids early in life may impinge on subsequent fight performance and consequently afect the dynamics of house invasion and reinfestation, and the efectiveness of triatomine control operations.

Improved vector control of Triatoma infestans limited by emerging pyrethroid resistance across an urban-to-rural gradient in the Argentine Chaco

Background: The sustainable elimination of Triatoma infestans in the Gran Chaco region represents an enduring challenge. Following the limited effects of a routine pyrethroid insecticide spraying campaign conducted over 2011­2013 (first period) in Avia Terai, an endemic municipality with approximately 2300 houses, we implemented a rapid-impact intervention package to suppress house infestation across the urban-to-rural gradient over 2015­2019 (second period). Here, we assess their impacts and whether persisting infestations were associated with pyrethroid resistance. Methods: The 2011­2013 campaign achieved a limited detection and spray coverage across settings (< 68%), more so during the surveillance phase. Following community mobilization and school-based interventions, the 2015­2019 program assessed baseline house infestation using a stratified sampling strategy; sprayed all rural houses with suspension concentrate beta-cypermethrin, and selectively sprayed infested and adjacent houses in urban and peri-urban settings; and monitored house infestation and performed selective treatments over the follow-up. Results: Over the first period, house infestation returned to pre-intervention levels within 3­4 years. The adjusted relative odds of house infestation between 2011­2013 and 2015­2016 differed very little (adj. OR: 1.17, 95% CI 0.91­1.51). Over the second period, infestation decreased significantly between 0 and 1 year post-spraying (YPS) (adj. OR: 0.36, 95% CI 0.28­0.46), with heterogeneous effects across the gradient. Mean bug abundance also dropped between 0 and 1 YPS and thereafter remained stable in rural and peri-urban areas. Using multiple regression models, house infestation and bug abundance at 1 YPS were 3­4 times higher if the house had been infested before treatment, or was scored as high-risk or non-participating. No low-risk house was ever infested. Persistent foci over two successive surveys increased from 30.0 to 59.3% across the gradient. Infestation was more concentrated in peridomestic rather than domestic habitats. Discriminating-dose bioassays showed incipient or moderate pyrethroid resistance in 7% of 28 triatomine populations collected over 2015­2016 and in 83% of 52 post-spraying populations. Conclusions: The intervention package was substantially more effective than the routine insecticide spraying campaign, though the effects were lower than predicted due to unexpected incipient or moderate pyrethroid resistance. Increased awareness and diagnosis of vector control failures in the Gran Chaco, including appropriate remedial actions, are greatly needed.

Recuperação rápida da infestação domiciliar por Triatoma brasiliensis após pulverização residual de inseticida em região semiárida do Nordeste do Brasil / Fast recovery of house infestation with Triatoma brasiliensis after residual insecticide spraying in a semiarid region of Northeastern Brazil

The northeastern semiarid region stands out in the Brazilian context regarding the eco-epidemiology of Chagas disease, in which Triatoma brasiliensis is the main vector of Trypanosoma cruzi. Persistent house invasion threatens the relative levels of progress achieved over previous decades. We conducted an intervention trial with a five-year follow-up to assess the impacts of residual spraying with pyrethroid insecticides on house infestation with T. brasiliensis in 18 rural villages (242 houses) located in the Tauá, Ceará. House infestations were assessed by systematic manual searches for triatomines in every domestic and peridomestic habitat on five occasions. Triatomines were collected in peridomestic (57.5%), sylvatic (35.8%), and intradomiciliary (6.7%) habitats. The most important ecotopes of T. brasiliensis were containing roofing tiles, bricks or rocks (23.4% ± 9.1). Residual insecticide spraying substantially reduced baseline house infestation rates from 27.9% to 5.9% by 6 months post first spraying (MPS). The decline was substantially greater in intradomiciles (11.2% to 0.8%) than in peridomiciles (16.7% to 5%). The mean relative density of triatomines recovered its preintervention values at 14 MPS in intradomiciles, and in the main peridomestic ecotopes. The house infestation levels recorded at 14 MPS persisted thereafter despite all reinfested houses were selectively sprayed on every occasion. Overall average bug infection rates with T. cruzi in the five occasions were in intradomiciles (11.1%), peridomiciles (4.7%) and wild habitats (3.3%). In peridomicile T. cruzi infection rates decreased significantly at all stages after chemical intervention. In intradomicile, the only significant difference occurred at 20 MPS (7.7% to 30.8%). The vectorial capacity of T. brasiliensis, combined with its invasive potential from sylvatic sources and the limited effectiveness of chemical control in the harsh caatinga landscape, pose serious obstacles to the definite elimination of domestic transmission risks. Systematic vector surveillance supported by community participation and locally adapted environmental management measures are needed to reduce the risks of establishment of domestic transmission with T. cruzi in this region.

Fast recovery of house infestation with Triatoma brasiliensis after residual insecticide spraying in a semiarid region of Northeastern Brazil

The northeastern semiarid region stands out in the Brazilian context regarding the eco-epidemiology of Chagas disease, in which Triatoma brasiliensis is the main vector of Trypanosoma cruzi. Persistent house invasion threatens the relative levels of progress achieved over previous decades. We conducted an intervention trial with a five-year follow-up to assess the impacts of residual spraying with pyrethroid insecticides on house infestation with T. brasiliensis in 18 rural villages (242 houses) located in the Tauá, Ceará. House infestations were assessed by systematic manual searches for triatomines in every domestic and peridomestic habitat on five occasions. Triatomines were collected in peridomestic (57.5%), sylvatic (35.8%), and intradomiciliary (6.7%) habitats. The most important ecotopes of T. brasiliensis were containing roofing tiles, bricks or rocks (23.4% ± 9.1). Residual insecticide spraying substantially reduced baseline house infestation rates from 27.9% to 5.9% by 6 months post first spraying (MPS). The decline was substantially greater in intradomiciles (11.2% to 0.8%) than in peridomiciles (16.7% to 5%). The mean relative density of triatomines recovered its preintervention values at 14 MPS in intradomiciles, and in the main peridomestic ecotopes. The house infestation levels recorded at 14 MPS persisted thereafter despite all reinfested houses were selectively sprayed on every occasion. Overall average bug infection rates with T. cruzi in the five occasions were in intradomiciles (11.1%), peridomiciles (4.7%) and wild habitats (3.3%). In peridomicile T. cruzi infection rates decreased significantly at all stages after chemical intervention. In intradomicile, the only significant difference occurred at 20 MPS (7.7% to 30.8%). The vectorial capacity of T. brasiliensis, combined with its invasive potential from sylvatic sources and the limited effectiveness of chemical control in the harsh caatinga landscape, pose serious obstacles to the definite elimination of domestic transmission risks. Systematic vector surveillance supported by community participation and locally adapted environmental management measures are needed to reduce the risks of establishment of domestic transmission with T. cruzi in this region.

Fluctuating asymmetry and exposure to pyrethroid insecticides in Triatoma infestans populations in northeastern Argentina

Fluctuating asymmetry (FA), a phenotypic marker used as indicator of developmental stress or instability, is sometimes associated with insecticide application and resistance. Here we investigated the occurrence and amount of wing size and wing shape FA in Triatoma infestans females and males collected before and 4 months after a community-wide pyrethroid spraying campaign in a well-defined rural area of Pampa del Indio, Argentina. Moderate levels of pyrethroid resistance were previously confirmed for this area, and postspraying house infestation was mainly attributed to this condition. In the absence of insecticide-based selective pressures over the previous 12 years, we hypothesized that 1- if postspraying triatomines were mostly survivors to insecticide spraying (pyrethroid resistant), they would have higher levels of FA than prespraying triatomines. 2- if postspraying triatomines have a selective advantage, they would have lower FA levels than their prespraying counterparts, whereas if postspraying infestation was positively associated with immigrants not exposed to the insecticide, prespraying and postspraying triatomines would display similar FA levels. For 243 adult T. infestans collected at identified sites before insecticide spraying and 112 collected 4 months postspraying, wing size and wing shape asymmetry was estimated from landmark configurations of left and right sides of each individual. At population level, wing size and shape FA significantly decreased in both females and males after spraying. Males displayed greater wing size and shape FA than females. However, at a single peridomestic site that was persistently infested after spraying, FA declined similarly in females whereas the reverse pattern occurred in males. Our results suggest differential survival of adults with more symmetric wings. This pattern may be related to a selective advantage of survivors to insecticide spraying, which may be mediated or not by their pyrethroid-resistant status or to lower triatomine densities after insecticide spraying and the concomitant increase in feeding success.

The eco-epidemiology of Triatoma infestans in the temperate Monte Desert ecoregion of mid-western Argentina

BACKGROUND The eco-epidemiological status of Chagas disease in the Monte Desert ecoregion of western Argentina is largely unknown. We investigated the environmental and socio-demographic determinants of house infestation with Triatoma infestans, bug abundance, vector infection with Trypanosoma cruzi and host-feeding sources in a well-defined rural area of Lavalle Department in the Mendoza province. METHODS Technical personnel inspected 198 houses for evidence of infestation with T. infestans, and the 76 houses included in the current study were re-inspected. In parallel with the vector survey, an environmental and socio-demographic survey was also conducted. Univariate risk factor analysis for domiciliary infestation was carried out using Firth penalised logistic regression. We fitted generalised linear models for house infestation and bug abundance. Blood meals were tested with a direct ELISA assay, and T. cruzi infection was determined using a hot-start polymerase chain reaction (PCR) targeting the kinetoplast minicircle (kDNA-PCR). FINDINGS The households studied included an aged population living in precarious houses whose main economic activities included goat husbandry. T. infestans was found in 21.2% of 198 houses and in 55.3% of the 76 re-inspected houses. Peridomestic habitats exhibited higher infestation rates and bug abundances than did domiciles, and goat corrals showed high levels of infestation. The main host-feeding sources were goats. Vector infection was present in 10.2% of domiciles and 3.2% of peridomiciles. Generalised linear models showed that peridomestic infestation was positively and significantly associated with the presence of mud walls and the abundance of chickens and goats, and bug abundance increased with the number of all hosts except rabbits. MAIN CONCLUSIONS We highlight the relative importance of specific peridomestic structures (i.e., goat corrals and chicken coops) associated with construction materials and host abundance as sources of persistent bug infestation driving domestic colonisation. Environmental management strategies framed in a community-based programme combined with improved insecticide spraying and sustained vector surveillance are needed to effectively suppress local T. infestans populations.

A motorized vehicle-mounted sprayer as a new tool for Chagas disease vector control / Equipamiento aspersor montado en vehículos como nueva herramienta para el control vectorial de la enfermedad de Chagas / Equipamento aspersor montado em veículo como ferramenta nova para o controle vetorial da doença de Chagas

Abstract: Residual insecticide spraying still is the main tool used to suppress house infestations with Chagas disease vectors. While manual compression sprayers (MCS) have traditionally been used in Latin America, Mendoza's vector control program from Argentina introduced the use of a modified motorized vehicle-mounted sprayer (VMS) with apparent advantages over MCS. We conducted a randomized intervention trial to evaluate the effectiveness and selected components of the performance of MCS and VMS. We assessed house infestation by Triatoma infestans in 76 previously-infested houses at 0, 1, 4 and 12 months postintervention. Infestations were reduced substantially, with no significant differences between treatments. End-point infestations were restricted to peridomiciles. Although VMS required less time to complete the house spraying than MCS, both treatments had similar performance and did not suppress infestations completely. The main relative advantages of VMS were a reduced physical effort, especially under harsh field conditions, and potential gains in spray coverage per unit of time.

Resumen: El empleo de insecticida residual es todavía la principal herramienta para suprimir la infestación domiciliaria por triatominos, vectores de la enfermedad de Chagas. Mientras los aspersores manuales activados por compresión han sido utilizados tradicionalmente en América Latina, el programa de control vectorial de la provincia de Mendoza, Argentina, introdujo el uso de un equipamiento aspersor montado en un vehículo, aparentemente con ventajas respecto al aspersor manual. Realizamos un ensayo de intervención aleatorizado para evaluar la efectividad y los componentes seleccionados del desempeño de los dos equipamientos. Evaluamos la infestación por Triatoma infestans en 76 vivendas, previamente infestados a 0, 1, 4 y 12 meses tras la intervención. Las infestaciones se redujeron substancialmente, sin diferencia significativa entre las dos técnicas. Las infestaciones finales se limitaban al peridomicilio. El equipamiento montado en el vehículo llevaba menos tiempo para completar la aplicación, comparado con el equipamiento manual, pero los dos tratamientos tuvieron un desempeño semejante y dejaron de suprimir completamente las infestaciones. Las principales ventajas del equipamiento montado en vehículo fueron: la reducción del esfuerzo físico, principalmente en condiciones adversas en el campo, y potenciales beneficios en términos de cobertura de pulverización por unidad de tiempo.

Resumo: A aplicação de inseticida residual ainda é a principal medida para suprimir a infestação domiciliar por triatomíneos, vetores da doença de Chagas. Enquanto os aspersores manuais acionados por compressão têm sido utilizados tradicionalmente na América Latina, o programa de controle vetorial da Província de Mendoza, Argentina, introduziu o uso de um equipamento aspersor montado em veículo, aparentemente com vantagem em relação ao aspersor manual. Realizamos um estudo randomizado de intervenção para avaliar a efetividade e os componentes selecionados do desempenho dos dois equipamentos. Avaliamos a infestação por Triatoma infestans em 76 domicílios previamente infestados a 0, 1, 4 e 12 meses pós-intervenção. As infestações foram reduzidas substancialmente, sem diferença significativa entre as duas técnicas. As infestações finais eram limitadas ao peridomicílio. O equipamento montado em veículo levava menos tempo para completar a aplicação, comparado com o equipamento manual, mas os dois tratamentos tiveram desempenho semelhante e deixaram de suprimir completamente as infestações. As principais vantagens do equipamento montado em veículo foram redução do esforço físico, principalmente em condições adversas em campo, e potenciais ganhos em termos de cobertura de borrifação por unidade de tempo.

Where do these bugs come from? Phenotypic structure of Triatoma infestans populations after control interventions in the Argentine Chaco

House re-invasion by native triatomines after insecticide-based control campaigns represents a major threat for Chagas disease vector control. We conducted a longitudinal intervention study in a rural section (Area III, 407 houses) of Pampa del Indio, northeastern Argentina, and used wing geometric morphometry to compare pre-spray and post-spray (re-infestant bugs) Triatoma infestans populations. The community-wide spraying with pyrethroids reduced the prevalence of house infestation by T. infestans from 31.9% to < 1% during a four-year follow-up, unlike our previous studies in the neighbouring Area I. Two groups of bug collection sites differing in wing shape variables before interventions (including 221 adults from 11 domiciles) were used as a reference for assigning 44 post-spray adults. Wing shape variables from post-spray, high-density bug colonies and pre-spray groups were significantly different, suggesting that re-infestant insects had an external origin. Insects from one house differed strongly in wing shape variables from all other specimens. A further comparison between insects from both areas supported the existence of independent re-infestation processes within the same district. These results point to local heterogeneities in house re-infestation dynamics and emphasise the need to expand the geographic coverage of vector surveillance and control operations to the affected region.